Readmissions Following Pancreaticoduodenectomy: Experience From a Tertiary Care Center in India

Background An enhanced recovery approach in surgery helps early postoperative discharge. With the decreasing trend of morbidity and mortality in recent times in patients undergoing complex procedures such as pancreaticoduodenectomy, readmissions are the next major concern. The causes and outcomes of these readmissions should be investigated for their impact on patient care and prevention. Methodology A total of 997 patients discharged after pancreaticoduodenectomy from a tertiary care center in northern India, between 1989 and 2021, were studied retrospectively to assess the readmission rate for sequelae after pancreaticoduodenectomy. The causes, interventions, outcomes, and predictive factors were studied. Results A total of 103 (10.3%) patients required readmission for sequelae after pancreaticoduodenectomy, and 52 (50.4%) patients required interventions. The most common cause for readmission in our study was intra-abdominal collection (n = 23, 22.3%). Of these 103 patients, 63 (61.2%) had good outcomes, 36 (34.9%) had fair outcomes, and four (3.9%) had bad outcomes. Overall, 53 (51.5%) of 103 patients were readmitted within 30 days of discharge, most commonly with intra-abdominal collection (16 of 53, 30.1%). Of these 53 patients, 22 (41.5%) required interventions, 34 (64.1%) had good outcomes, and 27 (50.9%) were readmitted within seven days of discharge. Of these 27 patients, 12 (44.4%) required interventions, with 24 (88.8%) experiencing good outcomes. Of the 103 patients, 12 (11.6%) were readmitted between 31 and 90 days, mostly due to external stent, T-tube, or percutaneous transhepatic biliary drainage-related problems. Overall, 38 (36.9%) of 103 patients were readmitted after 90 days, mostly with incisional hernia and strictured hepaticojejunostomy. Of these 38 patients, 26 (68.4%) required intervention, and 23 (60.5%) had good outcomes. A previous history of cholangitis (odds ratio (OR) = 1.771, 95% confidence interval (CI) = 1.17-2.67, p = 0.007), postoperative fever (OR = 1.628, 95% CI = 1.081-2.452, p = 0.02), wound infection (OR = 2.011, 95% CI = 1.332-3.035, p = 0.001), and wound dehiscence (OR = 2.136, 95% CI = 1.333-3.423, p = 0.002) predicted readmission on univariate analysis. Multivariate analysis showed a previous history of cholangitis (OR = 1.755, CI = 1.158-2.659, p = 0.008) and wound infection (OR = 1.995, 95% CI = 1.320-2.690, p = 0.001) as factors independently predicting readmission. Conclusions Readmitted patients have high intervention rates and good recovery rates. Readmissions should not be considered a scale for poor healthcare. Patient education, proper management of postoperative complications, and a properly designed discharge care system can help tackle this problem.


Introduction
Improved perioperative care has decreased the mortality and morbidity of surgical procedures.Mortality rates have decreased from 20% to 5% over the last few decades, and some institutes have documented nearzero mortality, defined as less than 2% [1,2].Morbidity decreased from 40% to 23% in many centers [2].Regionalization has contributed significantly to improving patient care for complex procedures such as pancreaticoduodenectomy (PD) [3,4].Better understanding of the disease, enhanced imaging services, proper patient selection, advanced surgical equipment, enhanced perioperative care, and better management of postoperative complications have improved patients' quality of life.Enhanced recovery approaches have aided in early postoperative discharge.In this context, readmissions become important because they decrease the quality of life, add anxiety to patients, and contribute to extra burden to the healthcare system [5].A thorough understanding of the clinical profile of patients who are readmitted can throw light on the prevention of readmissions.In procedures such as PD, which has inbuilt high rates of morbidity, readmissions have a major impact.The primary aim and objective of this study is to analyze the incidence, causes, and outcomes of patients readmitted after PD because of surgical sequelae.In this study, we hypothesized that patient demographics, preoperative status, intraoperative details, and postoperative complications might have an association with readmissions following PD.The study also aimed at identifying factors that can predict readmissions and methods to address the problem.
The preliminary results of this paper were presented as a poster at HBP Surgery Week 2021 and the 54th Annual Congress of the Korean Association of HBP Surgery, virtually held on March 25-27, 2021, at the Grand Walkerhill Hotel, Seoul, Korea.
All patients who were discharged after PD (index surgery) from our institute and who required readmission for sequelae of surgery were included in the study retrospectively.Patients readmitted for tumor recurrence, chemotherapy-related causes, and readmissions unrelated to the index surgery were excluded.Patients readmitted to outside hospitals were also excluded.
Preoperative biliary drainage was indicated in patients with cholangitis, poor performance status, locally advanced disease, and high bilirubin as per the choice of the treating surgeon.Preoperative preparation of the patient, surgical technique, and postoperative management of complications were guided by departmental guidelines.These guidelines were regularly updated based on the recent literature available at that time.The definition and grading of complications was based on the updated International Study Group in Pancreatic Surgery guidelines at that time.Surgically placed intra-abdominal drains were analyzed according to the clinical status of the patients in the postoperative period.Intra-abdominal drain removal was done when the drain output was less than 30 mL per day and as per the decision of the treating surgeon based on the clinical condition of the patients.Patients were discharged postoperatively at the decision of the treating surgeon when the patients were afebrile (less than 99.5°F for two days), had stable inflammatory parameters on blood investigations, well-established nutrition, adequate pain control with oral analgesia, and compliant with the discharge advice at home.
Patients readmitted for sequelae of the index surgery were grouped based on the period of readmission: within 30 days of discharge, 31 to 90 days of discharge, and more than 90 days following discharge.The causes, interventions, and outcomes of each group were analyzed.Outcomes of readmissions were grouped as good (if both symptomatic and biochemical improvement were present), fair (if either symptomatic or biochemical improvement were present), and bad (if the condition of the patient deteriorated either symptomatically or biochemically).
Patients readmitted because of sequelae (group 1) of the index surgery were analyzed and compared with patients who were not readmitted (group 2) with respect to demographic features, clinical presentation, intraoperative details of the index surgery, disease pathology, and postoperative complications.Patients on regular medications for any of the diseases, i.e., coronary heart disease, valvular heart disease, pre-existing liver disease or renal disease, or lung parenchymal disease, were considered to have medical risk factors affecting mortality.Factors determining readmission were analyzed using univariate and multivariate analysis.Our institute's experience with readmissions following PD for the study duration (1989-2021) was presented in a quinquennially time frame.Yearly readmission rates were also analyzed and presented appropriately.

Statistical analysis
Statistical analysis was done using SPSS Statistics Version 20 (IBM Corp., Armonk, NY, USA).Continuous variables were presented in mean ± SD, and a comparison of means between the two groups was done by an independent t-test.Categorical variables were presented as numbers (%).Univariate binary logistic regression analysis was used to identify the variables that were significantly associated with the readmission of the patients.All significant variables in univariate analysis were tested using the chi-square test for the multicollinearity and were not significantly associated with each other.These variables were further included in the multivariate binary logistic regression analysis.Unadjusted odds ratio (OR) and adjusted odds ratio along with a 95% confidence interval (CI) were used to present the results of the univariate and multivariate analysis respectively.P-values less than 0.05 were considered statistically significant.

Results
Of the 997 patients, 103 (10.3%) were readmitted (group 1) because of sequelae related to the index surgery.These patients (group 1, n = 103) had an average postoperative hospital stay of 20.74 days (SD = 14.35) during their index surgery.Patients who were not readmitted (group 2, n = 894) had an average postoperative hospital stay of 17.74 days (SD = 11.61) with a p-value of 0.014.Table 1 enumerates the causes of readmissions due to sequelae of index surgery and the intervention requirement for each cause of readmission.The most common cause for readmission in our study was intra-abdominal collection (n = 23, 22.3%).Overall, 52 (50.4%) of 103 patients required intervention during readmission.Of these 103 readmitted patients, 63 (61.2%) had good outcomes, 36 (34.9%) had fair outcomes, and four (3.9%) had bad outcomes.The average hospital stay during readmission was 13 days (range = 1-150 days).No mortality was documented.

Causes of readmissions
Frequency (n = 103) Intervention requirement in each cause of readmission (n = frequency in that particular cause, by %)    Of these 53 patients, 27 (50.9%)were readmitted within seven days after discharge.The most common cause for readmission was intra-abdominal collection (n = 7, 25.9%) in these patients.Out of 27 patients, 12 (44.4%)required intervention, with PCD (n = 6, 50%) being the most common intervention.The average hospital stay of these patients was 12.2 days (range = 1-40 days); 24 of 27 (88.8%)patients had good outcomes, whereas three of 27 (11.1%)had fair outcomes.

Our experience
The quinquennial readmission rate is depicted in Table 7.As the volume of patients discharged from our institute increased, our readmission rate for sequelae of surgery initially increased (the maximum five-year readmission rate was 11.8%) and then decreased.The yearly readmission rate is plotted in Figure 1.

Discussion
In our study, 10.3% of patients required readmission following PD, for causes related to sequelae of the index surgery, with intra-abdominal collection being the most common cause.Most of these readmitted patients (50.4%) required intervention.Overall, 61.2% of readmitted patients had good outcomes.The intraabdominal collection was the most common cause of readmission within 30 days after discharge post-PD, with PCD and UGIE being the common interventions required.External stent, T-tube, or PTBD-related problems were the most common causes of readmission within 31 to 90 days following discharge.Readmission after 90 days following discharge was mostly due to an incisional hernia.In our study, factors such as a previous history of cholangitis and wound infection independently predicted readmission.
Readmissions after PD are attributed to multiple causes related to a primary disease, post-surgical complications, and adjuvant therapy.These readmissions can occur in different time frames.The readmission rate after PD varied from 11.6% to 59% [6][7][8][9].This wide variation can be attributed to varied inclusion criteria in different studies.Our study focused on readmissions due to surgical sequelae following PD, with an overall readmission rate of 10.3% (103 out of 997) comparable to the reported range of 11.6% to 17% [9][10][11].
About half (27 out of 53, 50.9%) of the patients who required readmission within 30 days were readmitted within seven days after discharge.This group had a high intervention rate (12 out of 27, 44.4%) and most patients had good outcomes (24 out of 27, 88.8%).Fong et al. [15], also determined that 50% of all readmissions occurred within seven days after discharge (early readmission) with ileus, DGE, and pneumonia as the most common causes.Ahmad et al. [12] reported that 6% of their readmissions occurred within seven days and believed that "these early readmissions (readmission within seven days) could be avoided with proper anticipation of complications and by attaching skilled nursing staff to these patients."We followed our patients with postoperative complications within seven days after discharge, which helped us identify patients who may have needed life-saving intervention.Early follow-ups can avoid mortality, as reflected in our study.In resource-poor centers such as ours, educating patients' caretakers during hospital stays almost compensated for the lack of skilled nursing staff.
Of those readmissions (12 out of 103, 11.6%) that occurred between 31 and 90 days following discharge, 50% (six of 12) were related to external stents, T-tubes, or PTBD-related problems and wound-related complications, as depicted in Table 3. Judicious use of stents and PTBD can prevent readmissions related to complications such as blockage, slippage, and dislodgement.Failure to thrive was found to be a common cause of readmissions between 31 and 90 days in some studies [12,13].Nutritional education for patients and their caretakers can help address this problem.
Very few studies focused on the long-term causes of readmissions following PD.Of our readmissions, 36.9% (38 out of 103) occurred 90 days following discharge, and the most common cause was incisional hernia (eight out of 38, 21.1%), as found in other studies [10].Most of the patients (60.5%) readmitted after 90 days after discharge had good outcomes in our study, as depicted in Table 4. Kastenberg et al. [5] noted readmission rates of 27.4% within six months and 37.4% within one year of discharge, but the causes of readmission were not mentioned.Reddy et al. [6] reported that 25% of their late readmissions (30 days to within 1 year) were related to operative complications.Hari et al. [16] studied 90-day readmission rates after PD and found dehydration and malnutrition to be the major causes of readmission.This study determined that "self-care education" provided to patients and attendees could decrease preventable readmissions and that the best time for this self-care education would be in the preoperative period.
Kent et al. [17] found that 14% of their patients were readmitted for some clinical concern but did not find any complications on workup.Kastenberg et al. [5] reported 8% of patients with negative diagnostic workups.We have an "observation room facility" at our department, where patients are monitored and reassessed after six to eight hours with biochemical and imaging workups, which helps avoid unnecessary readmissions.
The intervention requirement and outcomes during readmissions have not been studied previously.Our study showed an overall intervention rate of 50.4% (52 out of 103), and 61.2% (63 out of 103) patients had good outcomes.Only 3.9% (four out of 103) had bad outcomes.Readmitted patients had high intervention requirements, some even life-saving.If treated effectively, the results should be satisfactory.Readmissions should not be considered as a burden on the healthcare system because they provide an opportunity to improve patient care.
Patient-related factors such as age, gender, and comorbidities were not associated with readmission risk in our study, consistent with other studies [5,12,15,[17][18][19].Some studies [9,14,20] reported higher readmission rates in younger patients, which may be attributed to "extensive dissections" performed in younger patients leading to increased complications.Although some studies [11,14,21,22] reported readmissions to be significantly associated with patients with comorbidities, we found no such association in our study.These variations in different studies could be due to differences in samples.
The patients' condition at the time of discharge was studied to predict readmission in some studies."Nonroutine discharge (discharge with home health services or discharge to nursing or rehabilitation facility)," as described by Kastenberg et al. [5], was associated with 30-day readmission (OR = 2.69, 95% CI = 1.17-6.12).The presence of pancreatic leak [23] at discharge and discharge with drain [13] were also predictors of readmission.
Does the length of the hospital stay during the index surgery predict readmission?In our study, patients who required readmission had significantly longer postoperative hospital stays during their index surgery (mean = 20.74days, SD = 14.35) compared to those not readmitted (mean = 17.74 days, SD = 11.61,p = 0.014).Prolonged hospital stays during index surgery have been identified as a risk factor for readmission by many studies [3,6,7,11,13,14,20].Patients who require a prolonged hospital stay during an index procedure are the ones who suffer complications, and it is imperative to be aware that these patients might return after discharge.
In our study, early discharge (discharge within 10 days after surgery) was not found to affect readmission (OR = 0.434, 95% CI = 0.488-1.361,p = 0.434), as reported in other studies [7,17,24].Balzano et al. [24] found that patients with a "fast track perioperative care program" after PD had shorter hospital stays (p < 0.001) but no significant change in the readmission rate (7.1% versus 6.3%, p = 0.865).Hospitals should develop their own criteria for discharge, and patients fulfilling those criteria can be discharged as early as possible, without any fear of readmission.Ceppa et al. [25] showed that a "reengineered discharge checklist" decreased the readmission rate from 23% to 15-19%.We discharge patients when they are sepsis-free, have well-established nutritional access, and are compliant with discharge advice.Patients' caretakers have an important role to play, so they should be well-educated about nutrition, wound care, and warning signs in the early postoperative period.Many studies focused on the effect of readmission on the survival of patients.Although some studies [26] showed decreased survival in patients who required readmissions, in our study, readmissions did not affect survival, similar to other studies [5,12,17].
Many studies [3,4,21] have focused on the effect of hospital volume on outcomes for patients undergoing PD.Some centers [2] showed improved patient care and outcomes as their experience in performing PD increased.Patients requiring PD should be referred to high-volume centers to lower readmissions and improve healthcare [3].High-volume institutions should formulate steps for tackling readmissions in this era of modern surgery.In our institution, as the volume of PD increased, the readmission rate increased initially (the highest five-year readmission rate was 21%).With improved postoperative care and well-planned discharge policies, the readmission rate decreased (7.7%) despite an increased volume (Table 7, Figure 1).We identify and enroll one caretaker (from patients' attendants) for each patient who undergoes PD and train them in wound care, nutritional support, and warning symptoms from the early postoperative period.This step has prevented nutrition-related readmissions.Well-educated caretakers bring patients with warning symptoms early to the hospital, decreasing mortality.
Our study focused on patients who were readmitted for both early and late consequences following PD, whereas most previous studies focused only on early consequences.We were unique in reporting the intervention rate of readmissions and outcomes of patients readmitted in different time frames, which most previous studies have not focused on.We included a homogenous sample of patients who were readmitted for sequelae after PD.
The study had its own demerit in that it was retrospective.The study period was of more than three decades (1989 to 2021).Over this long duration, the changes in patient approach, surgical techniques, postoperative care, and hospital policies might influenced our results.The underreporting of readmission rates is a concern in hospital-based studies [6] because some readmissions can occur in secondary hospitals [11].As a tertiary referral center, our surgical patients who required readmission were referred back to our institution, but readmissions in secondary hospitals in our study are a possibility.Because patients in emergencies might not have had access to our hospital, a major limitation of this study is that our readmissions might have been underestimated.

Conclusions
Readmission for sequelae after PD is a significant health problem.Most of these readmissions occur within 30 days after discharge.Most of these patients require intervention, and some interventions can be lifesaving.Readmitted patients have good outcomes despite the need for intervention.Patients who suffered postoperative complications are at a high risk of readmission and frequent follow-ups in these patients can decrease them.A well-planned discharge and properly designed post-discharge care systems can help reduce readmissions.Patients' caretakers should be educated about nutrition management and wound care, and this education should be started in the early postoperative period.Readmissions should not be considered a scale for poor healthcare because they help decrease 30-day post-discharge mortality.

FIGURE 1 :
FIGURE 1: Plot showing the yearly trend of readmissions for the sequelae of surgery regarding patients discharged after pancreaticoduodenectomy (the drop in cases in 2019 was due to the COVID-19 pandemic).